Abstract
Background, aim, and scope
Trace elements (heavy metals and metalloids) are important environmental pollutants, and many of them are toxic even at very low concentrations. Pollution of the biosphere with trace elements has accelerated dramatically since the Industrial Revolution. Primary sources are the burning of fossil fuels, mining and smelting of metalliferous ores, municipal wastes, agrochemicals, and sewage. In addition, natural mineral deposits containing particularly large quantities of heavy metals are found in many regions. These areas often support characteristic plant species thriving in metal-enriched environments. Whereas many species avoid the uptake of heavy metals from these soils, some of them can accumulate significantly high concentrations of toxic metals, to levels which by far exceed the soil levels. The natural phenomenon of heavy metal tolerance has enhanced the interest of plant ecologists, plant physiologists, and plant biologists to investigate the physiology and genetics of metal tolerance in specialized hyperaccumulator plants such as Arabidopsis halleri and Thlaspi caerulescens. In this review, we describe recent advances in understanding the genetic and molecular basis of metal tolerance in plants with special reference to transcriptomics of heavy metal accumulator plants and the identification of functional genes implied in tolerance and detoxification.
Results
Plants are susceptible to heavy metal toxicity and respond to avoid detrimental effects in a variety of different ways. The toxic dose depends on the type of ion, ion concentration, plant species, and stage of plant growth. Tolerance to metals is based on multiple mechanisms such as cell wall binding, active transport of ions into the vacuole, and formation of complexes with organic acids or peptides. One of the most important mechanisms for metal detoxification in plants appears to be chelation of metals by low-molecular-weight proteins such as metallothioneins and peptide ligands, the phytochelatins. For example, glutathione (GSH), a precursor of phytochelatin synthesis, plays a key role not only in metal detoxification but also in protecting plant cells from other environmental stresses including intrinsic oxidative stress reactions. In the last decade, tremendous developments in molecular biology and success of genomics have highly encouraged studies in molecular genetics, mainly transcriptomics, to identify functional genes implied in metal tolerance in plants, largely belonging to the metal homeostasis network.
Discussion
Analyzing the genetics of metal accumulation in these accumulator plants has been greatly enhanced through the wealth of tools and the resources developed for the study of the model plant Arabidopsis thaliana such as transcript profiling platforms, protein and metabolite profiling, tools depending on RNA interference (RNAi), and collections of insertion line mutants. To understand the genetics of metal accumulation and adaptation, the vast arsenal of resources developed in A. thaliana could be extended to one of its closest relatives that display the highest level of adaptation to high metal environments such as A. halleri and T. caerulescens.
Conclusions
This review paper deals with the mechanisms of heavy metal accumulation and tolerance in plants. Detailed information has been provided for metal transporters, metal chelation, and oxidative stress in metal-tolerant plants. Advances in phytoremediation technologies and the importance of metal accumulator plants and strategies for exploring these immense and valuable genetic and biological resources for phytoremediation are discussed.
Recommendations and perspectives
A number of species within the Brassicaceae family have been identified as metal accumulators. To understand fully the genetics of metal accumulation, the vast genetic resources developed in A. thaliana must be extended to other metal accumulator species that display traits absent in this model species. A. thaliana microarray chips could be used to identify differentially expressed genes in metal accumulator plants in Brassicaceae. The integration of resources obtained from model and wild species of the Brassicaceae family will be of utmost importance, bringing most of the diverse fields of plant biology together such as functional genomics, population genetics, phylogenetics, and ecology. Further development of phytoremediation requires an integrated multidisciplinary research effort that combines plant biology, genetic engineering, soil chemistry, soil microbiology, as well as agricultural and environmental engineering.
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References
Alscher RG (1989) Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant 77:457–464
Arrick BA, Nathan CF, Griffith OW, Cohn ZA (1982) Glutathione depletion sensitizes tumor cells to oxidative cytolysis. J Biol Chem 257:1231–1237
Assunçao AGL, Schat H, Aarts MGM (2003) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyper-accumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:181–126
Baker AJM, Walker PL (1990) Ecophysiology of metal uptake by tolerant plants, heavy metal tolerance in plants. In: Shaw AJ (ed) Evolutionary aspects. CRC, Boca Raton, pp 155–177
Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biochemical resource for phytoremediation of metal-polluted soils. In: Terry N, Bañuelos G, Vangronsveld J (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, USA, pp 85–107
Banuelos GS, Meek DW (1990) Accumulation of selenium in plants grown on selenium-treated soil. J Environ Qual 19:727–777
Becher M, Talke IN, Krall L, Kramer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268
Bennett LE, Burkhead JL, Hale KL, Terry N, Pilon M, Pilon-Smits EAH (2003) Analysis of transgenic Indian mustard plants for phytoremediation of metal contaminated, mine tailings. J Environ Qual 32:432–440
Bereczky Z, Wang HY, Schubert V, Ganal M, Bauer P (2003) Differential regulation of Nramp and IRT metal transporter genes in wild type and iron uptake mutants of tomato. J Biol Chem 278:24697–24704
Bernal M, Testillano PS, Alfonso M, Del Carmen Risueno M, Picorel R, Yruela I (2007) Identification and subcellular localization of the soybean copper P1B-ATPase GmHMA8 transporter. J Struct Biol 158:146–158
Bernard C, Roosens N, Czernic P, Lebrun M, Verbruggen N (2004) A novel CPxATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett 569:140–148
Blaudez D, Kohler A, Martin F, Sanders D, Chalot M (2003) Poplar metal tolerance protein 1 confers zinc tolerance and is an oligomeric vacuolar zinc transporter with an essential leucine zipper motif. Plant Cell 15:2911–2928
Bratteler M, Lexer C, Widmer A (2006) Genetic architecture of traits associated with serpentine adaptation of Silene vulgaris. J Evol Biol 19:1149–1156
Brooks RR (1983) Biological methods of prospecting for minerals. Wiley, New York
Campbell EJ, Schenk PM, Kazan K, Penninckx IAMA, Anderson JP, Maclean DJ, Cammue BPA, Ebert PR, Manners JM (2003) Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid Sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiol 133:1272–1284
Chiang HC, Lo JC, Yeh KC (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyper-accumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ Sci Technol 40:6792–6798
Clemens S (2001) Molecular mechanisms of plant metal hoemostatsis. Planta 212:475–486
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719
Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthase from plants and yeast. EMBO J 18:3325–3333
Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins, roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182
Cobbett S, Meagher RB (2002) Arabidopsis and the genetic potential for the phytoremediation of toxic elemental and organic pollutants. The Arabidopsis book. American Society of Plant Biologists, ISNN 1543–8120, http://www.org/publications/arabidopsis open access pp 1–22
Cosio C, Martinoia E, Keller C (2004) Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis hallari at the leaf cellular level. Plant Physiol 134:716–725
Coupe SA, Taylor JE, Roberts JA (1995) Characterization of an m-RNA encoding a metallothionein-like protein that accumulates during ethylene-promoted abscission of Sambucus nigra L. Planta 197:442–447
Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065
David-Assael O, Berezin I, Shoshani-Knaani N, Saul H, Mizrachy-Dagri T, Chen J, Brook E, Shaul O (2006) AtMHX is an auxin and ABA-regulated transporter whose expression pattern suggests a role in metal homeostasis in tissues with photosynthetic potential. Funct Plant Biol 33:661–672
Deniau AX, Pieper B (2006) WMT-B, QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920
Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138:2233–2244
Domenech J, Mir G, Huguet G, Capdevila M, Molinas M, Atrian S (2006) Plant metallothionein domains: functional insight into physiological metal binding and protein folding. Biochimie 88:583–593
Drager DB, Desbrosses-Fonrouge AG, Krach C, Chardonnens AN, Meyer RC, Saumitou-Laprade P, Kramer U (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39:425–439
Ducruix C, Junot C, Fievet JB, Villiers F, Ezan E, Bourguignon J (2006) New insights into the regulation of phytochelatin biosynthesis in A. thaliana cells from metabolite profiling analyses. Biochimie 88:1733–1742
EC (2002) Towards a thematic strategy for soil protection. COM 179 final. European Commission, Brussels, Belgium
EEA (2003) Europe’s environment: the third assessment. Environmental assessment report no. 10. European Environment Agency, Copenhagen, Denmark
Ensley BD (2000) Rationale for use of phytoremediation pp. 3–11. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. J. Wiley & Sons, New York, USA, 304 pp
Fernando DR, Woodrow IE, Jaffre T, Dumontet V, Marshall AT, Baker AJM (2007) Foliar manganese accumulation by Maytenus founieri (Celastraceae) in its native New Caledonian habitats: populational variation and localization by X-ray microanalysis. New Phytol 177:178–185
Filatov V, Dowdle J, Smirnoff N (2006) Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation. Mol Ecol 15:3045–3059
Filatov V, Dowdle J, Smirnoff N, Ford-Lloyd B, Newbury HJ, Macnair MR (2007) A quantitative trait loci analysis of zinc hyperaccumulation in Arabidopsis halleri. New Phytol 174:580–590
Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signaling. Physiol Plant 100:241–254
Franzius V (1994) Aktuelle Entwicklungen zur Altlastenproblematik in der Bundesrepublik Deutschland. Umwelt Technologie Aktuell 6:443–449
Freeman JL, Salt DE (2007) The metal tolerance profile of Thlaspi goesingense is mimicked in Arabdopsis thaliana heterologously expressing serine acetyl-transferase. BMC Plant Biol 7(63):1–10
Gaither LA, Eide DJ (2001) Eukaryotic zinc transporters and their regulation. Biometals 14:251–270
Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194
Ghandilyan A, Vreugdenhil D, Aarts MGM (2006) Progress in the genetic understanding of plant iron and zinc nutrition, nutriomics and biofortification. Physiol Plant 126:407–417
Glass DJ (2000) Economic potential of phytoremediation. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 15–31
Grant CM, Maclver FH, Dawes IW (1996) Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr Genet 29:511–515
Grill E, Löffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy metals-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamilcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci U S A 86:6838–6842
Guo WJ, Meetam M, Goldsbrough P (2008) Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 164(4):1697–1706
Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connel MJ, Goldsborough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast, Schizosaccaromyces pombe. Plant Cell 11:1153–1164
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613
Hammond JP, Bowen HC, White PJ, Mills V, Pyke KA, Baker AJM (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol 170:239–260
Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395
Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113
Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133
Hodoshima H, Enomoto Y, Shoji K, Shimada H, Goto F, Yoshihara T (2007) Differential regulation of cadmium-inducible expression of iron-deficiency-responsive genes in tobacco and barley. Physiol Plant 129:622–634
Howden R, Goldsbrough PB, Andersen CR, Cobbett CS (1995) Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol 107:1059–1066
Hsieh HM, Liu WK, Huang PC (1995) A novel stress-inducible metallothionein-like gene from rice. Plant Mol Biol 28:381–389
Hussain D, Michael JH, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbet CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339
Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) OsZIP4, a novel zinc-regulated zinc transporter in rice. J Exp Bot 56:3207–214
Kawachi M, Kobae Y, Mimura T, Maeshima M (2008) Deletion of a histidine-rich loop of AtMTP1, a vacuolar Zn2+/H+ antiporter of Arabidopsis thaliana, stimulates the transport activity. J Biol Chem 283:8374–8383
Kerkeb L, Mukherjee I, Chatterjee I, Lahner B, Salt DE, Connolly EL (2008) Iron-induced turnover of the Arabidopsis iron-regulated transporter1 metal transporter requires lysine residues. Plant Physiol 146:1964–1973
Kim D, Gustin JL, Lahner B, Persans MW, Baek D, Yun DJ, Salt DE (2004) The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae. Plant J 39:237–251
Kim DY, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:1–11
Lanquar V, Lelievre F, Bolte S, Hames C, Alcon C, Neumann D, Vansuyt G, Curie C, Schröder A, Kramer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNramp3 and AtNramp4 is essential for seed germination on low iron. EMBO J 24:4041–4051
Ledger SE, Gardner RC (1994) Cloning and characterization of five cDNAs for genes differentially expressed during fruit development of kiwifruit (Actinia deliciosa var deliciosa). Plant Mol Biol 25:877–886
Lee S, Kim Y-Y, Lee Y, An G (2007) Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol 145:831–842
Lewandowski U, Schmidt M, Londo A, Faaij (2006) The economic value of the phytoremediation function—assessed by the example of cadmium remediation by willow (Salix ssp). Agric Syst 89(1):68–89 (July)
Lopez-Millan AF, Ellis DR, Grusak MA (2004) Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Mol Biol 54:583–596
Maathuis FJM, Filatov V, Krijger GC, Herzyk P, Axelsen KB (2003) Transcriptome analysis of Arabidopsis thaliana cation transport. Plant J 35:675–692
Macnair MR (1993) The genetic of metal tolerance in vascular plants. New Phytol 124:541–559
Marmiroli N, Maestri E (2008) Health implications of trace elements in the environment and the food chain. In: Prasad MNV (ed) Trace elements as contaminants and nutrients—consequences in ecosystems and human health. Wiley, New Jersey, USA, pp 23–53
Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667
Maughan S, Foyer CH (2006) Genetic approaches to modulating the glutathione network in plants, nutriomics and biofortification. Physiol Planta 126:382–397
May MJ, Leaver CJ (1995) Arabidopsis thaliana g-glutamylcysteine synthetase is structurally unrelated to mammalian, yeast and Escherichia coli homologues. Proc Natl Acad Sci U S A 91:10059–10063
McGrath SP, Lombi E, Gray CW, Caille N, Dunham SJ, Zhao FJ (2006) Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environ Pollut 141:115–125
Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760
Memon AR, Yatazawa M (1982) Chemical nature of manganese in the leaves of manganese accumulator plants. Soil Sci Plant Nutr 28:401–412
Memon AR, Yatazawa M (1984) Nature of manganese complexes in Mn accumulator plant—Acanthopanax sciadophylloides. J Plant Nutr 7:961–974
Memon AR, Chino M, Yatazawa M (1981) Microdistribution of aluminum and manganese in the tea leaf tissue as revealed by X-ray microanalyzer. Commun Soil Sci Plant Nutr 27:317–328
Memon AR, Aktoprakligıl D, Özdemir A, ve Vertii A (2000) Heavy metal accumulation and detoxification mechanisms in plants. Turk J Bot 25:111–121
Memon AR, Yildizhan Y, Demirel U (2006) Cu tolerance and accumulation in Brassica nigra and development of in vitro regeneration system for phytoremediation. COST action 859: phytotechnologies to promote sustainable land use and improve food safety. WG2 and WG3 workshop -omics approaches and agricultural management: driving forces to improve food quality and safety? Universite Jean Monnet et Ecole Nationale Superieure des Mines, Saint-Etienne, France, pp 37–38
Memon AR, Yildizhan Y, Keskin BC (2008a) Enhanced Cu tolerance in Brassica nigra (L.) is associated with increased transcription level of γ-glutamylcysteine synthatase (γ-ECS) and phytochelatin synthase (PCS). COST action 859: genes and proteins involved in steps of phytoextraction and degradation of pollutants, workshop WG2: exploiting “-omics” approaches in phytotechnologies. University of Verona, Verona, Italy, p 68
Memon AR, Yildizhan Y, Kaplan E (2008b) Metal accumulation in crops—human health issue. In: Prasad MNV (ed) Trace elements as contaminants and nutrients—consequences in ecosystems and human health. Wiley, New Jersey, USA, pp 81–98
Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13
Mirouze M, Sels J, Richard O, Czernic P, Loubet S, Jacquier A, Francois IEJA, Cammue BPA, Lebrun M, Berthomieu P, Marques L (2006) A putative novel role for plant defensins: a defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant J 47:329–342
Moreau S, Thomson RM, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, Puppo A, Day DA (2002) GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J Biol Chem 277:4738–4746
Morris CA, Nicolaus B, Sampson V, Harwood JL, Kille P (1999) Identification and characterization of a recombinant metallothionein protein from a marine alga, Fucus vesiculosus. Biochem J 338:553–560
Murphy A, Taiz L (1995) Comparison of metallothionein gene expression and non-protein thiols in 10 Arabidopsis ecotypes correlation with copper tolerance. Plant Physiol 109:1–10
Murphy A, Zhou J, Goldsbrough PB, Taiz L (1997) Purification and immunological identification of metallothioneins 1and 2 from Arabidopsis thaliana. Plant Physiol 113:1293–1301
Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647
Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454
Ortiz DF, Russcitti T, McCuc KF, Ow DW (1995) Transport of metal binding peptides by HMT1, a fission yeast ABC type vacuolar membrane protein. J Biol Chem 27:4721–4728
Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyper accumulation of metals in plants. Water Air Soil Pollut 184:105–126
Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136:3814–3823
Pence NS, Larsen PB, Ebbs SD, Letham DL, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci U S A 97:4956–4960
Pilson-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39
Plaza S, Tearall KL, Zhao FJ, Buchner P, McGrath SP, Hawkesford MJ (2007) Expression and functional analysis of metal transporter genes in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 58:1717–1728
Prasad MNV (2008) Trace elements as contaminants and nutrients—consequences in ecosystems and human health. Wiley, New Jersey, USA
Rauser WE (1990) Phytochelatins. Annu Rev Biochem 59:61–86
Rauser WE (1999) Structure and function of metal chelators produced by plants; the case for organic acids, amino acids, phytin and metallothioneins. Cell Biochem Biophys 31:19–48
Rauser WE (2000) Roots of maize seedlings retain most of their cadmium through two complexes. J Plant Physiol 156:545–551
Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375
Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediat 3:145–172
Rigola D, Fiers M, Vurro E, Aarts MGM (2006) The heavy metal hyperaccumulator Thlaspi caerulescens expresses many species-specific genes, as identified by comparative expressed sequence tag analysis. New Phytol 170:753–766
Robinson NJ, Tommey AM, Kuske C, Jackson PJ (1993) Plant metallothioneins. Biochem J 295:1–10
Rogers EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14:1787–1799
Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci 97:12356–12360
Roosens N, Bernard C, Leplae R, Verbruggen N (2004) Evidence for copper homeostasis function of metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens. FEBS Lett 577:9–16
Roosens NH, Leplae R, Bernard C, Verbruggen N (2005) Variations in plant metallothioneins: the heavy metal hyperaccumulator Thlaspi caerulescens as a study case. Planta 222:716–729
Roosens NHCJ, Willems G, Saumitou-Laprade P (2008) Using Arabidopsis to explore zinc tolerance and hyperaccumulation. Trends Plant Sci 13:208–215
Rüegsegger A, Brunold C (1992) Effect of cadmium on g-glutamylcysteine synthesis in maize seedlings. Plant Physiol 99:428–433
Sahi SV, Bryant NL, Sharma NC, Singh SR (2002) Characterization of lead hyperaccumulator shrub, Sesbania drummondii. Environ Sci Technol 36:4676–4680
Salt DE, Blaylock M, Kumar PBAN, Dushenkov S, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474
Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668
Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, Inze D, May MJ (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc Natl Acad Sci U S A 94:2745–2750
Sanchez-Fernandez R, Emyr Davies TG, Coleman JOD, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily a complete inventory. J Biol Chem 276:30231–30244
Sarry J-E, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O, Fievet JB, Vailhen D, Amerkraz B, Moulin C, Ezan E, Garin J, Bourguignon (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198
Schat H, Ten Bookum WM (1992) Genetic control of copper tolerance in Silene vulgaris. Heredity 68:219–229
Schneider A, Bergmann L (1995) Regulation of glutathione synthesis in suspension cultures of parsley and tobacco. Bot Acta 108:34–40
Schröder P (2007) Exploiting plant metabolism for phytoremediation of organic xenobiotics. In: Willey N (ed) Phytoremediation: methods and reviews. Humana, New Jersey, USA
Schröder P, Navarro Avino J, Azaizeh H, Golan Goldhirsh A, DiGregorio S, Komives T, Langergraber G, Lenz A, Maestri E, Memon A, Ranalli A, Sebastiani L, Smrcek S, Vanek T, Vuillemier S, Wissing F (2007) Position paper: using phytoremediation technologies to upgrade waste water treatment in Europe. Environ Sci Pollut Res Int 14:490–497
Schröder P, Herzig R, Bojnov B, Ruttens A, Nehnevajova E, Stamatiadis S, Memon AR, Vassilev A, Caviezel M, Vangronsveld J (2008) Bioenergy to save the world—novel plants for bioenergy production. Environ Sci Pollut Res Int 15:196–204
Shaul O, Mironov V, Burssens S, Van Montagu MV, Inze D (1996) Two Arabidopsis cyclin promoters mediate distinctive transcriptional oscillation in synchronised tobacco 3Y-2 cells. Proc Natl Acad Sci U S A 93:4868–4872
Shingu Y, Kudo T, Ohsato S, Kimura M, Ono Y, Yamaguchi I, Hamamoto H (2005) Characterization of genes encoding metal tolerance proteins isolated from Nicotiana glauca and Nicotiana tabacum. Biochem Biophys Res Commun 331:675–680
Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2006) Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol 140:613–623
Stearns JC, Shah S, Glick BR (2007) Increasing plant tolerance to metals in the environment. In: Willey N (ed) Methods in biotechnology. Phytoremediation. Methods and review. vol. 23. Humana, New Jersey, pp 15–26
Talke IN, Kramer U, Hanikenne M (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167
Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci 97:4991–4996
Tong YP, Kneer R, Zhu YG (2004) Vacuolar compartmentalization: a second generation approach to engineering plants for phytoremediation. Trends Plant Sci 9:7–9
Van de Mortel JE (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147
Vatamanuik OK, Mari S, Lu YP, Rea PA (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci 96:7110–7115
Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richand P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of Zn and Cd and plant metal tolerance. FEBS Lett 576:306–312
Verrier P, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EJ, Yazaki K, Theodoulou FL (2008) Plant ABC proteins—a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159
Vestergaard M, Matsumoto S, Nishikori S, Shiraki K, Hirata K, Takagi M (2008) Chelation of cadmium ions by phytochelatin synthase: role of the cystein-rich C-terminal. Anal Sci 24:277–281
Wang C, Oliver DJ (1996) Cloning of the cDNA and genomic clones for glutathione synthetase from Arabidopsis thaliana and complementation of gsh2 mutant in fission yeast. Plant Mol Biol 31:1093–1104
Wangeline AL, Burkhead JL, Hale KL, Lindblom SD, Terry N, Pilon M, Pilon-Smits EAH (2004) Overexpression of ATP sulfurylase in Indian mustard: effects on tolerance and accumulation of 12 metals. J Environ Qual 33:54–60
Weber M, Harada E, Vess C, Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotinamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281
Wei S, Zhou Q (2008) Trace elements in agro-ecosystems. In: Prasad MNV (ed) Trace elements as contaminants and nutrients—consequences in ecosystems and human health. Wiley, New Jersey, USA, pp 55–80
Welch RM, Graham RD (2003) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364
Whiting SN, Reeves RD, Richards D, Johnson MS, Cooke JA, Malaisse F, Paton A, Smith JAC, Angle JS, Chaney RL, Ginocchio R, Jaffré T, Johns R, McIntyre T, Purvis OW, Salt DE, Schat H, Zhao FJ, Baker AJM (2004) Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restor Ecol 12:106–116
Willems G, Dräger DB, Courbot M (2007) The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. Halleri (Brassicaceae) an analysis of quantitative trait loci. Genetics 176:659–674
Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 1465:104–126
Wintz H, Fox T, Wu YY, Feng V, Chen W, Chang HS, Zhu T, Vulpe C (2003) Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem 278:47644–47653
Xing JP, Jiang RF, Ueno D, Ma JF, Schat H, McGrath SP, Zhao FJ (2008) Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox. New Phytol 178:315–325
Zhou J, Goldsbrough PB (1994) Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell 6:875–884
Zhou GK, Xu YF, Liu JY (2005) Characterization of a rice class II metallothionein gene: tissue expression patterns and induction in response to abiotic factors. J Plant Physiol 162:686–696
Zhu LY, Pilon-Smits EAH, Jouanin L, Terry N (1999a) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:73–79
Zhu LH, Pilon-Smits EAH, Tarun AS, Weber SU, Jouanin L, Terry N (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol 121:1169–1177
Acknowledgements
This work is part of the cooperation between groups working in a COST589 program. We extend our thanks to Dr. Jean-Paul Schwitzguebel for his encouragement and support for cooperation among COST 859 groups. We appreciate the comments of Dr. Oktay Külen and Gülten Güneş for some parts of the review.
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Memon, A.R., Schröder, P. Implications of metal accumulation mechanisms to phytoremediation. Environ Sci Pollut Res 16, 162–175 (2009). https://doi.org/10.1007/s11356-008-0079-z
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DOI: https://doi.org/10.1007/s11356-008-0079-z